D-amino acid metabolic versatility as a common adaptive strategy in the Mariana Trench microbiome

ABSTRACT Hadal trenches, the Earth’s deepest marine environments, harbor thriving microbial communities that promote the turnover of recalcitrant dissolved organic matter (RDOM) under extreme conditions. However, the effects of microbes on D-amino acid (D-AA) reservoirs, which are important components of deep-sea RDOM, remain largely unknown. To address this knowledge gap, we curated a comprehensive reference database of D-AA functional genes for accurate identification of D-AA metabolic potential from metagenomic data. Using this database, we identified the presence of various D-AA anabolic and catabolic genes that were closely correlated with central carbon metabolism and ammonia oxidation genes throughout the water column and in the sediment of the Mariana Trench. Furthermore, 93.6% of the recovered bacterial and archaeal genomes contained at least one of these D-AA functional genes, substantially expanding our understanding of potential D-AA utilizers. Notably, we discovered that glutamate racemase, an enzyme previously thought to be exclusive to bacteria, is ubiquitously present in ammonia-oxidizing archaea. This finding suggests that D-glutamate could be integrated into hadal carbon and nitrogen cycling by this crucial microbial taxon. Finally, we observed an increase in both D-AA production and degradation potential with water depth, with higher levels in near-bottom seawater than in sediment. These findings suggest that diverse microbial taxa promote increased D-AA turnover in hadal zones, potentially representing a common adaptive response to extreme hadal conditions. IMPORTANCE Deep-sea microorganisms play a crucial role in the turnover of RDOM. In this study, we investigated the metabolic potential of D-AAs, which are important constituents of RDOM and are used for indicating the recalcitrance of organic matter. By elucidating the genetic profiles of D-AA metabolism and associated microbial taxa, we observed that D-AA metabolism is a fundamental ecological function that is prevalent in the deepest ocean. Our finding of higher D-AA turnover potentials in deeper environments challenges the conventional view of the constant recalcitrance of D-AAs, suggesting that D-AA turnover may be environmentally dependent. This insight provides a new paradigm for understanding RDOM turnover, with broad implications for marine biogeochemistry.